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Erschienen in: e-Neuroforum 4/2016

28.11.2016 | Review article

Cajal-Retzius cells: organizers of cortical development

verfasst von: Werner Kilb, Michael Frotscher

Erschienen in: e-Neuroforum | Ausgabe 4/2016

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Abstract

Cajal-Retzius cells (CRc) are a major neuronal population in the marginal zones of the developing neocortex and hippocampus. CRc belong to the earliest born neurons in the cortex and originate from several regions at the pallial-subpallial border. A substantial fraction of CRc disappears during postnatal development. CRc express a variety of neurotransmitter receptors, receive mainly GABAergic synaptic inputs and give rise to glutamatergic synapses. Recent studies identified some modes of how CRc are integrated into immature neuronal circuits, although their exact role for immature information processing remains unknown. As a major source for the extracellular matrix protein reelin, which is critically involved in lamination of the cerebral cortex, CRc are an important factor for the structural development of the neocortex and hippocampus. In addition, CRc contribute to the patterning of cortical areas and shape the development of perforant path connections in the hippocampus. In summary, CRc are a major cellular element in the structural development of the cerebral cortex and may serve as a link between early electrical activity and morphological organization during prenatal und early postnatal development.
Literatur
1.
Zurück zum Zitat Aboitiz F, Montiel J (2007) Origin and evolution of the vertebrate telencephalon, with special reference to the mammalian neocortex. Adv Anat Embryol Cell Biol 193:1–112CrossRefPubMed Aboitiz F, Montiel J (2007) Origin and evolution of the vertebrate telencephalon, with special reference to the mammalian neocortex. Adv Anat Embryol Cell Biol 193:1–112CrossRefPubMed
2.
Zurück zum Zitat Achilles K, Okabe A, Ikeda M, Shimizu-Okabe C, Yamada J, Fukuda A, Luhmann HJ, Kilb W (2007) Kinetic properties of Cl− uptake mediated by Na+-dependent K+-2Cl(−) cotransport in immature rat neocortical neurons. J Neurosci 27:8616–8627CrossRefPubMed Achilles K, Okabe A, Ikeda M, Shimizu-Okabe C, Yamada J, Fukuda A, Luhmann HJ, Kilb W (2007) Kinetic properties of Cl− uptake mediated by Na+-dependent K+-2Cl(−) cotransport in immature rat neocortical neurons. J Neurosci 27:8616–8627CrossRefPubMed
3.
Zurück zum Zitat Alcantara S, Ruiz M, D’Arcangelo G, Ezan F, De Lecea L, Curran T, Sotelo C, Soriano E (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18:7779–7799PubMed Alcantara S, Ruiz M, D’Arcangelo G, Ezan F, De Lecea L, Curran T, Sotelo C, Soriano E (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18:7779–7799PubMed
4.
Zurück zum Zitat Anstoetz M, Cosgrove KE, Hack I, Mugnaini E, Maccaferri G, Luebke JH (2013) Morphology, input-output relations and synaptic connectivity of Cajal-Retzius cells in layer 1 of the developing neocortex of CXCR4-EGFP mice. Brain Struct Funct 2:1–21 Anstoetz M, Cosgrove KE, Hack I, Mugnaini E, Maccaferri G, Luebke JH (2013) Morphology, input-output relations and synaptic connectivity of Cajal-Retzius cells in layer 1 of the developing neocortex of CXCR4-EGFP mice. Brain Struct Funct 2:1–21
5.
Zurück zum Zitat Anstoetz M, Huang H, Marchionni I, Haumann I, Maccaferri G, Luebke JHR (2016) Developmental profile, morphology, and synaptic connectivity of Cajal-Retzius cells in the postnatal mouse hippocampus. Cereb Cortex 26:855–872 Anstoetz M, Huang H, Marchionni I, Haumann I, Maccaferri G, Luebke JHR (2016) Developmental profile, morphology, and synaptic connectivity of Cajal-Retzius cells in the postnatal mouse hippocampus. Cereb Cortex 26:855–872
6.
Zurück zum Zitat Barber M, Arai Y, Morishita Y, Vigier L, Causeret F, Borello U, Ledonne F, Coppola E, Contremoulins V, Pfrieger FW, Tissir F, Govindan S, Jabaudon D, Proux-Gillardeaux V, Galli T, Pierani A (2015) Migration speed of Cajal-Retzius cells modulated by vesicular trafficking controls the size of higher-order cortical areas. Curr Biol 25:2466–2478CrossRefPubMed Barber M, Arai Y, Morishita Y, Vigier L, Causeret F, Borello U, Ledonne F, Coppola E, Contremoulins V, Pfrieger FW, Tissir F, Govindan S, Jabaudon D, Proux-Gillardeaux V, Galli T, Pierani A (2015) Migration speed of Cajal-Retzius cells modulated by vesicular trafficking controls the size of higher-order cortical areas. Curr Biol 25:2466–2478CrossRefPubMed
7.
Zurück zum Zitat Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A (2005) Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 8:1002–1012CrossRefPubMed Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A (2005) Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 8:1002–1012CrossRefPubMed
8.
Zurück zum Zitat Blanquie O, Liebmann L, Hubner CA, Luhmann HJ, Sinning A (2016) NKCC1-mediated GABAergic signaling promotes postnatal cell death in neocortical Cajal-Retzius cells. Cereb Cortex. doi:10.1093/cercor/bhw004 PubMed Blanquie O, Liebmann L, Hubner CA, Luhmann HJ, Sinning A (2016) NKCC1-mediated GABAergic signaling promotes postnatal cell death in neocortical Cajal-Retzius cells. Cereb Cortex. doi:10.​1093/​cercor/​bhw004 PubMed
9.
Zurück zum Zitat Borrell V, Ruiz M, Del Río JA, Soriano E (1999) Development of commissural connections in the hippocampus of reeler mice: evidence of an inhibitory influence of Cajal-Retzius cells. Exp Neurol 156:268–282CrossRefPubMed Borrell V, Ruiz M, Del Río JA, Soriano E (1999) Development of commissural connections in the hippocampus of reeler mice: evidence of an inhibitory influence of Cajal-Retzius cells. Exp Neurol 156:268–282CrossRefPubMed
10.
Zurück zum Zitat Cajal SR (1891) Sur la structure de lecorce cerebrale de quelques mammiferes. Cellule 7:123–176 Cajal SR (1891) Sur la structure de lecorce cerebrale de quelques mammiferes. Cellule 7:123–176
11.
Zurück zum Zitat Ceranik K, Deng JB, Heimrich B, Lübke J, Zhao ST, Förster E, Frotscher M (1999) Hippocampal Cajal-Retzius cells project to the entorhinal cortex: retrograde tracing and intracellular labelling studies. Eur J Neurosci 11:4278–4290CrossRefPubMed Ceranik K, Deng JB, Heimrich B, Lübke J, Zhao ST, Förster E, Frotscher M (1999) Hippocampal Cajal-Retzius cells project to the entorhinal cortex: retrograde tracing and intracellular labelling studies. Eur J Neurosci 11:4278–4290CrossRefPubMed
12.
Zurück zum Zitat Chai X, Förster E, Zhao S, Bock HH, Frotscher M (2009) Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n‑cofilin phosphorylation at serine3. J Neurosci 29:288–299CrossRefPubMed Chai X, Förster E, Zhao S, Bock HH, Frotscher M (2009) Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n‑cofilin phosphorylation at serine3. J Neurosci 29:288–299CrossRefPubMed
13.
Zurück zum Zitat Chai X, Fan L, Shao H, Lu X, Zhang W, Li J, Wang J, Chen S, Frotscher M, Zhao S (2015) Reelin induces branching of neurons and radial glial cells during corticogenesis. Cereb Cortex 25:3640–3653CrossRefPubMed Chai X, Fan L, Shao H, Lu X, Zhang W, Li J, Wang J, Chen S, Frotscher M, Zhao S (2015) Reelin induces branching of neurons and radial glial cells during corticogenesis. Cereb Cortex 25:3640–3653CrossRefPubMed
14.
Zurück zum Zitat Chowdhury TG, Jimenez JC, Bomar JM, Cruz-Martin A, Cantle JP, Portera-Cailliau C (2010) Fate of Cajal-Retzius neurons in the postnatal mouse neocortex. Front Neuroanat 4:10PubMedPubMedCentral Chowdhury TG, Jimenez JC, Bomar JM, Cruz-Martin A, Cantle JP, Portera-Cailliau C (2010) Fate of Cajal-Retzius neurons in the postnatal mouse neocortex. Front Neuroanat 4:10PubMedPubMedCentral
15.
Zurück zum Zitat Cosgrove KE, Maccaferri G (2012) mGlu1 alpha-dependent recruitment of excitatory GABAergic input to neocortical Cajal-Retzius cells. Neuropharmacology 63:486–493CrossRefPubMedPubMedCentral Cosgrove KE, Maccaferri G (2012) mGlu1 alpha-dependent recruitment of excitatory GABAergic input to neocortical Cajal-Retzius cells. Neuropharmacology 63:486–493CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat D’Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719–723CrossRefPubMed D’Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719–723CrossRefPubMed
17.
Zurück zum Zitat Del Rio JA, Martinez A, Fonseca M, Auladell C, Soriano E (1995) Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. Cereb Cortex 5:13–21CrossRefPubMed Del Rio JA, Martinez A, Fonseca M, Auladell C, Soriano E (1995) Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretinin antibody. Cereb Cortex 5:13–21CrossRefPubMed
18.
Zurück zum Zitat Del Rio JA, Heimrich B, Borrell V, Förster E, Drakew A, Alcántara S, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Derer P, Frotscher M, Soriano E (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385:70–74CrossRefPubMed Del Rio JA, Heimrich B, Borrell V, Förster E, Drakew A, Alcántara S, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Derer P, Frotscher M, Soriano E (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385:70–74CrossRefPubMed
19.
Zurück zum Zitat Derer P, Derer M (1990) Cajal-Retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience 36:839–856CrossRefPubMed Derer P, Derer M (1990) Cajal-Retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience 36:839–856CrossRefPubMed
20.
Zurück zum Zitat Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES (2000) Reelin binds α3β1integrin and inhibits neuronal migration. Neuron 27:33–44CrossRefPubMed Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES (2000) Reelin binds α3β1integrin and inhibits neuronal migration. Neuron 27:33–44CrossRefPubMed
21.
Zurück zum Zitat Dvorzhak A, Unichenko P, Kirischuk S (2012) Glutamate transporters and presynaptic metabotropic glutamate receptors protect neocortical Cajal-Retzius cells against over-excitation. Pflugers Arch 464:217–225CrossRefPubMed Dvorzhak A, Unichenko P, Kirischuk S (2012) Glutamate transporters and presynaptic metabotropic glutamate receptors protect neocortical Cajal-Retzius cells against over-excitation. Pflugers Arch 464:217–225CrossRefPubMed
22.
Zurück zum Zitat Falconer DS (1951) Two new mutants ‘trembler’ and ‘reeler’ with neurological actions in the house mouse. J Genet 50:192–201CrossRefPubMed Falconer DS (1951) Two new mutants ‘trembler’ and ‘reeler’ with neurological actions in the house mouse. J Genet 50:192–201CrossRefPubMed
23.
Zurück zum Zitat Forster E, Zhao ST, Frotscher M (2006) Laminating the hippocampus. Nat Rev Neurosci 7:259–267CrossRefPubMed Forster E, Zhao ST, Frotscher M (2006) Laminating the hippocampus. Nat Rev Neurosci 7:259–267CrossRefPubMed
24.
Zurück zum Zitat Franco SJ, Martinez-Garay I, Gil-Sanz C, Harkins-Perry SR, Müller U (2011) Reelin Regulates Cadherin Function via Dab1/Rap1 to Control Neuronal Migration and Lamination in the Neocortex. Neuron 69(3):482–497CrossRefPubMedPubMedCentral Franco SJ, Martinez-Garay I, Gil-Sanz C, Harkins-Perry SR, Müller U (2011) Reelin Regulates Cadherin Function via Dab1/Rap1 to Control Neuronal Migration and Lamination in the Neocortex. Neuron 69(3):482–497CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Frotscher M (2010) Role for Reelin in stabilizing cortical architecture. Trends Neurosci 33:407–414CrossRefPubMed Frotscher M (2010) Role for Reelin in stabilizing cortical architecture. Trends Neurosci 33:407–414CrossRefPubMed
26.
Zurück zum Zitat Frotscher M, Haas CA, Förster E (2003) Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb Cortex 13:634–640CrossRefPubMed Frotscher M, Haas CA, Förster E (2003) Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb Cortex 13:634–640CrossRefPubMed
27.
Zurück zum Zitat Frotscher M, Chai XJ, Bock HH, Haas CA, Forster E, Zhao ST (2009) Role of Reelin in the development and maintenance of cortical lamination. J Neural Transm 116:1451–1455CrossRefPubMed Frotscher M, Chai XJ, Bock HH, Haas CA, Forster E, Zhao ST (2009) Role of Reelin in the development and maintenance of cortical lamination. J Neural Transm 116:1451–1455CrossRefPubMed
28.
Zurück zum Zitat Gil-Sanz C, Franco SJ, Martinez-Garay I, Espinosa A, Harkins-Perry S, Muller U (2013) Cajal-Retzius cells instruct neuronal migration by coincidence signaling between secreted and contact-dependent guidance cues. Neuron 79:461–477CrossRefPubMedPubMedCentral Gil-Sanz C, Franco SJ, Martinez-Garay I, Espinosa A, Harkins-Perry S, Muller U (2013) Cajal-Retzius cells instruct neuronal migration by coincidence signaling between secreted and contact-dependent guidance cues. Neuron 79:461–477CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Gil V, Nocentini S, Del Rio JA (2014) Historical first descriptions of Cajal-Retzius cells: from pioneer studies to current knowledge. Front Neuroanat 8:32CrossRefPubMedPubMedCentral Gil V, Nocentini S, Del Rio JA (2014) Historical first descriptions of Cajal-Retzius cells: from pioneer studies to current knowledge. Front Neuroanat 8:32CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Griveau A, Borello U, Causeret F, Tissir F, Boggetto N, Karaz S, Pierani A (2010) A novel role for Dbx1-derived Cajal-Retzius cells in early regionalization of the cerebral cortical neuroepithelium. PLOS Biol 8:e1000440CrossRefPubMedPubMedCentral Griveau A, Borello U, Causeret F, Tissir F, Boggetto N, Karaz S, Pierani A (2010) A novel role for Dbx1-derived Cajal-Retzius cells in early regionalization of the cerebral cortical neuroepithelium. PLOS Biol 8:e1000440CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat von Haebler D, Stabel J, Draguhn A, Heinemann U (1993) Properties of horizontal cells transiently appearing in the rat dentate gyrus during ontogenesis. Exp Brain Res 94:33–42CrossRef von Haebler D, Stabel J, Draguhn A, Heinemann U (1993) Properties of horizontal cells transiently appearing in the rat dentate gyrus during ontogenesis. Exp Brain Res 94:33–42CrossRef
32.
Zurück zum Zitat Gu XC, Liu B, Wu XJ, Yan Y, Zhang Y, Wei YQ, Pleasure SJ, Zhao CJ (2011) Inducible genetic lineage tracing of cortical hem derived Cajal-Retzius cells reveals novel properties. PLOS ONE 6:e28653CrossRefPubMedPubMedCentral Gu XC, Liu B, Wu XJ, Yan Y, Zhang Y, Wei YQ, Pleasure SJ, Zhao CJ (2011) Inducible genetic lineage tracing of cortical hem derived Cajal-Retzius cells reveals novel properties. PLOS ONE 6:e28653CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat Hamburgh M (1963) Analysis of postnatal developmental effects of reeler, a neurological mutation in mice - a study in developmental genetics. Dev Biol 8:165CrossRefPubMed Hamburgh M (1963) Analysis of postnatal developmental effects of reeler, a neurological mutation in mice - a study in developmental genetics. Dev Biol 8:165CrossRefPubMed
34.
Zurück zum Zitat Hestrin S, Armstrong WE (1996) Morphology and physiology of cortical neurons in layer I. J Neurosci 16:5290–5300PubMed Hestrin S, Armstrong WE (1996) Morphology and physiology of cortical neurons in layer I. J Neurosci 16:5290–5300PubMed
35.
Zurück zum Zitat Hevner RF, Neogi T, Englund C, Daza RA, Fink A (2003) Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Dev Brain Res 141:39–53CrossRef Hevner RF, Neogi T, Englund C, Daza RA, Fink A (2003) Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Dev Brain Res 141:39–53CrossRef
36.
Zurück zum Zitat Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481–489CrossRefPubMed Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, Herz J (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481–489CrossRefPubMed
37.
Zurück zum Zitat Honda T, Kobayashi K, Mikoshiba K, Nakajima K (2011) Regulation of cortical neuron migration by the Reelin signaling pathway. Neurochem Res 36:1270–1279CrossRefPubMed Honda T, Kobayashi K, Mikoshiba K, Nakajima K (2011) Regulation of cortical neuron migration by the Reelin signaling pathway. Neurochem Res 36:1270–1279CrossRefPubMed
38.
Zurück zum Zitat Ina A, Sugiyama M, Konno J, Yoshida S, Ohmomo H, Nogami H, Shutoh F, Hisano S (2007) Cajal-Retzius cells and subplate neurons differentially express vesicular glutamate transporters 1 and 2 during development of mouse cortex. Eur J Neurosci 26:615–623CrossRefPubMed Ina A, Sugiyama M, Konno J, Yoshida S, Ohmomo H, Nogami H, Shutoh F, Hisano S (2007) Cajal-Retzius cells and subplate neurons differentially express vesicular glutamate transporters 1 and 2 during development of mouse cortex. Eur J Neurosci 26:615–623CrossRefPubMed
39.
Zurück zum Zitat Janusonis S, Gluncic V, Rakic P (2004) Early serotonergic projections to Cajal-Retzius cells: relevance for cortical development. J Neurosci 24:1652–1659CrossRefPubMed Janusonis S, Gluncic V, Rakic P (2004) Early serotonergic projections to Cajal-Retzius cells: relevance for cortical development. J Neurosci 24:1652–1659CrossRefPubMed
40.
Zurück zum Zitat Jossin Y, Ignatova N, Hiesberger T, Herz J, Lambert DR, Goffinet AM (2004) The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci 24:514–521CrossRefPubMed Jossin Y, Ignatova N, Hiesberger T, Herz J, Lambert DR, Goffinet AM (2004) The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J Neurosci 24:514–521CrossRefPubMed
41.
Zurück zum Zitat Judas M, Sedmak G, Pletikos M (2010) Early history of subplate and interstitial neurons: from Theodor Meynert (1867) to the discovery of the subplate zone (1974). J Anat 217:344–367CrossRefPubMedPubMedCentral Judas M, Sedmak G, Pletikos M (2010) Early history of subplate and interstitial neurons: from Theodor Meynert (1867) to the discovery of the subplate zone (1974). J Anat 217:344–367CrossRefPubMedPubMedCentral
42.
Zurück zum Zitat Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Annu Rev Neurosci 33:23–48CrossRefPubMed Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Annu Rev Neurosci 33:23–48CrossRefPubMed
43.
Zurück zum Zitat Kilb W, Luhmann HJ (2000) Characterization of a hyperpolarization-activated inward current in Cajal-Retzius cells in rat neonatal neocortex. J Neurophysiol 84:1681–1691PubMed Kilb W, Luhmann HJ (2000) Characterization of a hyperpolarization-activated inward current in Cajal-Retzius cells in rat neonatal neocortex. J Neurophysiol 84:1681–1691PubMed
44.
Zurück zum Zitat Kilb W, Luhmann HJ (2001) Spontaneous GABAergic postsynaptic currents in Cajal-Retzius cells in neonatal rat cerebral cortex. Eur J Neurosci 13:1387–1390CrossRefPubMed Kilb W, Luhmann HJ (2001) Spontaneous GABAergic postsynaptic currents in Cajal-Retzius cells in neonatal rat cerebral cortex. Eur J Neurosci 13:1387–1390CrossRefPubMed
45.
Zurück zum Zitat Kilb W, Ikeda M, Uchida K, Okabe A, Fukuda A, Luhmann HJ (2002) Depolarizing glycine responses in Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 112:299–307CrossRefPubMed Kilb W, Ikeda M, Uchida K, Okabe A, Fukuda A, Luhmann HJ (2002) Depolarizing glycine responses in Cajal-Retzius cells of neonatal rat cerebral cortex. Neuroscience 112:299–307CrossRefPubMed
46.
Zurück zum Zitat Kilb W, Hartmann D, Saftig P, Luhmann HJ (2004) Altered morphological and electrophysiological properties of Cajal-Retzius cells in cerebral cortex of embryonic Presenilin-1 knockout mice. Eur J Neurosci 20:2749–2756CrossRefPubMed Kilb W, Hartmann D, Saftig P, Luhmann HJ (2004) Altered morphological and electrophysiological properties of Cajal-Retzius cells in cerebral cortex of embryonic Presenilin-1 knockout mice. Eur J Neurosci 20:2749–2756CrossRefPubMed
47.
Zurück zum Zitat Kirischuk S, Luhmann HJ, Kilb W (2014) Cajal-Retzius cells: update on structural and functional properties of these mystic neurons that bridged the 20th century. Neuroscience 275:33–46CrossRefPubMed Kirischuk S, Luhmann HJ, Kilb W (2014) Cajal-Retzius cells: update on structural and functional properties of these mystic neurons that bridged the 20th century. Neuroscience 275:33–46CrossRefPubMed
48.
Zurück zum Zitat Kirmse K, Grantyn R, Kirischuk S (2005) Developmental downregulation of low-voltage-activated Ca2+ channels in Cajal-Retzius cells of the mouse visual cortex. Eur J Neurosci 21:3269–3276CrossRefPubMed Kirmse K, Grantyn R, Kirischuk S (2005) Developmental downregulation of low-voltage-activated Ca2+ channels in Cajal-Retzius cells of the mouse visual cortex. Eur J Neurosci 21:3269–3276CrossRefPubMed
49.
Zurück zum Zitat Kirmse K, Dvorzhak A, Henneberger C, Grantyn R, Kirischuk S (2007) Cajal Retzius cells in the mouse neocortex receive two types of pre- and postsynaptically distinct GABAergic inputs. J Physiol 585:881–895CrossRefPubMedPubMedCentral Kirmse K, Dvorzhak A, Henneberger C, Grantyn R, Kirischuk S (2007) Cajal Retzius cells in the mouse neocortex receive two types of pre- and postsynaptically distinct GABAergic inputs. J Physiol 585:881–895CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Kolbaev SN, Achilles K, Luhmann HJ, Kilb W (2011) Effect of depolarizing GABA(A)-mediated membrane responses on excitability of Cajal-Retzius cells in the immature rat neocortex. J Neurophysiol 106:2034–2044CrossRefPubMed Kolbaev SN, Achilles K, Luhmann HJ, Kilb W (2011) Effect of depolarizing GABA(A)-mediated membrane responses on excitability of Cajal-Retzius cells in the immature rat neocortex. J Neurophysiol 106:2034–2044CrossRefPubMed
51.
Zurück zum Zitat Luhmann HJ, Reiprich RA, Hanganu IL, Kilb W (2000) Cellular physiology of the neonatal rat cerebral cortex: intrinsic membrane properties, sodium and calcium currents. J Neurosci Res 62:574–584CrossRefPubMed Luhmann HJ, Reiprich RA, Hanganu IL, Kilb W (2000) Cellular physiology of the neonatal rat cerebral cortex: intrinsic membrane properties, sodium and calcium currents. J Neurosci Res 62:574–584CrossRefPubMed
52.
Zurück zum Zitat Ma J, Yao XH, Fu Y, Yu YC (2013) Development of layer 1 neurons in the mouse neocortex. Cereb Cortex 24:2604–2618 Ma J, Yao XH, Fu Y, Yu YC (2013) Development of layer 1 neurons in the mouse neocortex. Cereb Cortex 24:2604–2618
53.
Zurück zum Zitat Marchionni I, Takacs VT, Nunzi MG, Mugnaini E, Miller RJ, Maccaferri G (2010) Distinctive properties of CXC chemokine receptor 4‑expressing Cajal-Retzius cells versus GABAergic interneurons of the postnatal hippocampus. JPhysiol 588:2859–2878CrossRefPubMedPubMedCentral Marchionni I, Takacs VT, Nunzi MG, Mugnaini E, Miller RJ, Maccaferri G (2010) Distinctive properties of CXC chemokine receptor 4‑expressing Cajal-Retzius cells versus GABAergic interneurons of the postnatal hippocampus. JPhysiol 588:2859–2878CrossRefPubMedPubMedCentral
54.
Zurück zum Zitat Magdaleno S, Keshvara L, Curran T (2002) Rescue of ataxia and preplate splitting by ectopic expression of reelin in reeler mice. Neuron 33:573–586CrossRefPubMed Magdaleno S, Keshvara L, Curran T (2002) Rescue of ataxia and preplate splitting by ectopic expression of reelin in reeler mice. Neuron 33:573–586CrossRefPubMed
55.
Zurück zum Zitat Marin-Padilla M (1990) Three-dimensional structural organization of layer I of the human cerebral cortex: a Golgi study. J Comp Neurol 299:89–105CrossRefPubMed Marin-Padilla M (1990) Three-dimensional structural organization of layer I of the human cerebral cortex: a Golgi study. J Comp Neurol 299:89–105CrossRefPubMed
56.
Zurück zum Zitat Marin-Padilla M (1998) Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 21:64–71CrossRefPubMed Marin-Padilla M (1998) Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 21:64–71CrossRefPubMed
57.
Zurück zum Zitat Marin-Padilla M (2015) Human cerebral cortex Cajal-Retzius neuron: development, structure and function. A Golgi study. Front Neuroanat 9:21PubMedPubMedCentral Marin-Padilla M (2015) Human cerebral cortex Cajal-Retzius neuron: development, structure and function. A Golgi study. Front Neuroanat 9:21PubMedPubMedCentral
59.
Zurück zum Zitat Martinez-Galan JR, Lopez-Bendito G, Lujan R, Shigemoto R, Fairen A, Valdeolmillos M (2001) Cajal-Retzius cells in early postnatal mouse cortex selectively express functional metabotropic glutamate receptors. Eur J Neurosci 13:1147–1154CrossRefPubMed Martinez-Galan JR, Lopez-Bendito G, Lujan R, Shigemoto R, Fairen A, Valdeolmillos M (2001) Cajal-Retzius cells in early postnatal mouse cortex selectively express functional metabotropic glutamate receptors. Eur J Neurosci 13:1147–1154CrossRefPubMed
60.
Zurück zum Zitat Martinez-Galan JR, Moncho-Bogani J, Caminos E (2014) Expression of calcium-binding proteins in layer 1 Reelin-immunoreactive cells during rat and mouse neocortical development. J Histochem Cytochem 62:60–69CrossRefPubMedPubMedCentral Martinez-Galan JR, Moncho-Bogani J, Caminos E (2014) Expression of calcium-binding proteins in layer 1 Reelin-immunoreactive cells during rat and mouse neocortical development. J Histochem Cytochem 62:60–69CrossRefPubMedPubMedCentral
61.
Zurück zum Zitat Meyer G, Goffinet AM (1998) Prenatal development of reelin-immunoreactive neurons in the human neocortex. J Comp Neurol 397:29–40CrossRefPubMed Meyer G, Goffinet AM (1998) Prenatal development of reelin-immunoreactive neurons in the human neocortex. J Comp Neurol 397:29–40CrossRefPubMed
62.
Zurück zum Zitat Meyer G, Goffinet AM, Fairén A (1999) What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. Cereb Cortex 9:765–775CrossRefPubMed Meyer G, Goffinet AM, Fairén A (1999) What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. Cereb Cortex 9:765–775CrossRefPubMed
63.
Zurück zum Zitat Meyer G, Perez-Garcia CG, Abraham H, Caput D (2002) Expression of p73 and Reelin in the developing human cortex. J Neurosci 22:4973–4986PubMed Meyer G, Perez-Garcia CG, Abraham H, Caput D (2002) Expression of p73 and Reelin in the developing human cortex. J Neurosci 22:4973–4986PubMed
64.
Zurück zum Zitat Meyer G, Cabrera SA, Perez Garcia CG, Martinez Millan L, Walker N, Caput D (2004) Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J Neurosci 24:9878–9887CrossRefPubMed Meyer G, Cabrera SA, Perez Garcia CG, Martinez Millan L, Walker N, Caput D (2004) Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J Neurosci 24:9878–9887CrossRefPubMed
65.
Zurück zum Zitat Mienville JM (1998) Persistent depolarizing action of GABA in rat Cajal-Retzius cells. J Physiol (Lond) 512:809–817CrossRef Mienville JM (1998) Persistent depolarizing action of GABA in rat Cajal-Retzius cells. J Physiol (Lond) 512:809–817CrossRef
66.
Zurück zum Zitat Mienville JM, Barker JL (1997) Potassium current expression during prenatal corticogenesis in the rat. Neuroscience 81:163–172CrossRefPubMed Mienville JM, Barker JL (1997) Potassium current expression during prenatal corticogenesis in the rat. Neuroscience 81:163–172CrossRefPubMed
67.
Zurück zum Zitat Mienville JM, Pesold C (1999) Low resting potential and postnatal upregulation of NMDA receptors may cause Cajal-Retzius cell death. J Neurosci 19:1636–1646PubMed Mienville JM, Pesold C (1999) Low resting potential and postnatal upregulation of NMDA receptors may cause Cajal-Retzius cell death. J Neurosci 19:1636–1646PubMed
68.
Zurück zum Zitat Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G (2010) Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582–1594CrossRefPubMedPubMedCentral Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G (2010) Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582–1594CrossRefPubMedPubMedCentral
69.
Zurück zum Zitat Muralidhar S, Wang Y, Markram H (2014) Synaptic and cellular organization of layer 1 of the developing rat somatosensory cortex. Front Neuroanat 7:52CrossRefPubMedPubMedCentral Muralidhar S, Wang Y, Markram H (2014) Synaptic and cellular organization of layer 1 of the developing rat somatosensory cortex. Front Neuroanat 7:52CrossRefPubMedPubMedCentral
70.
Zurück zum Zitat Myakhar O, Unichenko P, Kirischuk S (2011) GABAergic projections from the subplate to Cajal-Retzius cells in the neocortex. Neuroreport 22:525–529CrossRefPubMed Myakhar O, Unichenko P, Kirischuk S (2011) GABAergic projections from the subplate to Cajal-Retzius cells in the neocortex. Neuroreport 22:525–529CrossRefPubMed
71.
Zurück zum Zitat Ogawa M, Miyata T, Nakajimat K, Yagyu K, Seike M, Ikenaka K et al (1995) The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14(5):899–912CrossRefPubMed Ogawa M, Miyata T, Nakajimat K, Yagyu K, Seike M, Ikenaka K et al (1995) The reeler gene-associated antigen on cajal-retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14(5):899–912CrossRefPubMed
72.
Zurück zum Zitat Perez-Garcia CG, Gonzalez-Delgado FJ, Suarez-Sola ML, Castro-Fuentes R, Martin-Trujillo JM, Ferres-Torres R, Meyer G (2001) Reelin-immunoreactive neurons in the adult vertebrate pallium. J Chem Neuroanat 21:41–51CrossRefPubMed Perez-Garcia CG, Gonzalez-Delgado FJ, Suarez-Sola ML, Castro-Fuentes R, Martin-Trujillo JM, Ferres-Torres R, Meyer G (2001) Reelin-immunoreactive neurons in the adult vertebrate pallium. J Chem Neuroanat 21:41–51CrossRefPubMed
73.
Zurück zum Zitat Pozas E, Paco S, Soriano E, Aguado F (2008) Cajal-Retzius cells fail to trigger the developmental expression of the Cl(-)extruding co-transporter KCC2. Brain Res 1239:85–91CrossRefPubMed Pozas E, Paco S, Soriano E, Aguado F (2008) Cajal-Retzius cells fail to trigger the developmental expression of the Cl(-)extruding co-transporter KCC2. Brain Res 1239:85–91CrossRefPubMed
74.
Zurück zum Zitat Quattrocolo G, Maccaferri G (2013) Novel GABAergic circuits mediating excitation/inhibition of Cajal- Retzius cells in the developing hippocampus. J Neurosci 33:5486–5498CrossRefPubMedPubMedCentral Quattrocolo G, Maccaferri G (2013) Novel GABAergic circuits mediating excitation/inhibition of Cajal- Retzius cells in the developing hippocampus. J Neurosci 33:5486–5498CrossRefPubMedPubMedCentral
75.
Zurück zum Zitat Quattrocolo G, Maccaferri G (2014) Optogenetic activation of Cajal-Retzius cells reveals their glutamatergic output and a novel feedforward circuit in the developing mouse hippocampus. J Neurosci 34:13018–13032CrossRefPubMedPubMedCentral Quattrocolo G, Maccaferri G (2014) Optogenetic activation of Cajal-Retzius cells reveals their glutamatergic output and a novel feedforward circuit in the developing mouse hippocampus. J Neurosci 34:13018–13032CrossRefPubMedPubMedCentral
76.
Zurück zum Zitat Qian TZ, Chen RQ, Nakamura M, Furukawa T, Kumada T, Akita T, Kilb W, Luhmann HJ, Nakahara D, Fukuda A (2014) Activity-dependent endogenous taurine release facilitates excitatory neurotransmission in the neocortical marginal zone of neonatal rats. Frontiers Cell Neurosci 8:33CrossRef Qian TZ, Chen RQ, Nakamura M, Furukawa T, Kumada T, Akita T, Kilb W, Luhmann HJ, Nakahara D, Fukuda A (2014) Activity-dependent endogenous taurine release facilitates excitatory neurotransmission in the neocortical marginal zone of neonatal rats. Frontiers Cell Neurosci 8:33CrossRef
77.
Zurück zum Zitat Radnikow G, Feldmeyer D, Lübke J (2002) Axonal projection, input and output synapses, and synaptic physiology of Cajal-Retzius cells in the developing rat neocortex. J Neurosci 22:6908–6919PubMed Radnikow G, Feldmeyer D, Lübke J (2002) Axonal projection, input and output synapses, and synaptic physiology of Cajal-Retzius cells in the developing rat neocortex. J Neurosci 22:6908–6919PubMed
78.
Zurück zum Zitat Retzius G (1893) Die Cajal’schen Zellen der Grosshirnrinde beim Menschen und bei Säugetieren. Biol Untersuchungen 5:1–8 Retzius G (1893) Die Cajal’schen Zellen der Grosshirnrinde beim Menschen und bei Säugetieren. Biol Untersuchungen 5:1–8
79.
Zurück zum Zitat Sava BA, David CS, Teissier A, Pierani A, Staiger JF, Luhmann HJ, Kilb W (2010) Electrophysiological and morphological properties of Cajal-Retzius cells with different ontogenetic origins. Neuroscience 167:724–734CrossRefPubMed Sava BA, David CS, Teissier A, Pierani A, Staiger JF, Luhmann HJ, Kilb W (2010) Electrophysiological and morphological properties of Cajal-Retzius cells with different ontogenetic origins. Neuroscience 167:724–734CrossRefPubMed
80.
Zurück zum Zitat Schwartz TH, Rabinowitz D, Unni V, Kumar VS, Smetters DK, Tsiola A, Yuste R (1998) Networks of coactive neurons in developing layer 1. Neuron 20:541–552CrossRefPubMed Schwartz TH, Rabinowitz D, Unni V, Kumar VS, Smetters DK, Tsiola A, Yuste R (1998) Networks of coactive neurons in developing layer 1. Neuron 20:541–552CrossRefPubMed
81.
Zurück zum Zitat Soda T, Nakashima R, Watanabe D, Nakajima K, Pastan I, Nakanishi S (2003) Segregation and coactivation of developing neocortical layer 1 neurons. J Neurosci 23:6272–6279PubMed Soda T, Nakashima R, Watanabe D, Nakajima K, Pastan I, Nakanishi S (2003) Segregation and coactivation of developing neocortical layer 1 neurons. J Neurosci 23:6272–6279PubMed
82.
Zurück zum Zitat Soriano E, Del Rio JA (2005) The cells of Cajal-Retzius: still a mystery one century after. Neuron 46:389–394CrossRefPubMed Soriano E, Del Rio JA (2005) The cells of Cajal-Retzius: still a mystery one century after. Neuron 46:389–394CrossRefPubMed
83.
Zurück zum Zitat Soriano E, Del Rio JA, Martinez A, Super H (1994) Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. J Comp Neurol 342:571–595CrossRefPubMed Soriano E, Del Rio JA, Martinez A, Super H (1994) Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. J Comp Neurol 342:571–595CrossRefPubMed
84.
Zurück zum Zitat Stanfield BB, Cowan WM (1979) Morphology of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185:393–422CrossRefPubMed Stanfield BB, Cowan WM (1979) Morphology of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185:393–422CrossRefPubMed
85.
Zurück zum Zitat Super H, Martínez A, Del Río JA, Soriano E (1998) Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci 18:4616–4626PubMed Super H, Martínez A, Del Río JA, Soriano E (1998) Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci 18:4616–4626PubMed
86.
Zurück zum Zitat Tissir F, Ravni A, Achouri Y, Riethmacher D, Meyer G, Goffinet AM (2009) DeltaNp73 regulates neuronal survival in vivo. Proc Natl Acad Sci USA 106:16871–16876CrossRefPubMedPubMedCentral Tissir F, Ravni A, Achouri Y, Riethmacher D, Meyer G, Goffinet AM (2009) DeltaNp73 regulates neuronal survival in vivo. Proc Natl Acad Sci USA 106:16871–16876CrossRefPubMedPubMedCentral
87.
Zurück zum Zitat Tinnes S, Schafer MKE, Flubacher A, Munzner G, Frotscher M, Haas CA (2011) Epileptiform activity interferes with proteolytic processing of Reelin required for dentate granule cell positioning. FASEB J 25:1002–1013CrossRefPubMed Tinnes S, Schafer MKE, Flubacher A, Munzner G, Frotscher M, Haas CA (2011) Epileptiform activity interferes with proteolytic processing of Reelin required for dentate granule cell positioning. FASEB J 25:1002–1013CrossRefPubMed
88.
Zurück zum Zitat Trousse F, Poluch S, Pierani A, Dutriaux A, Bock HH, Nagasawa T, Verdier JM, Rossel M (2015) CXCR7 receptor controls the maintenance of subpial positioning of Cajal-Retzius cells. Cereb Cortex 25:3446–3457CrossRefPubMed Trousse F, Poluch S, Pierani A, Dutriaux A, Bock HH, Nagasawa T, Verdier JM, Rossel M (2015) CXCR7 receptor controls the maintenance of subpial positioning of Cajal-Retzius cells. Cereb Cortex 25:3446–3457CrossRefPubMed
89.
Zurück zum Zitat Valverde F, Facal-valverde MV, Santacana M, Heredia M (1989) Development and differentiation of early generated cells of sublayer VIb in the somatosensory cortex of the rat: A correlated Golgi and autoradiographic study. The Journal of Comparative Neurology 290 (1):118–140CrossRefPubMed Valverde F, Facal-valverde MV, Santacana M, Heredia M (1989) Development and differentiation of early generated cells of sublayer VIb in the somatosensory cortex of the rat: A correlated Golgi and autoradiographic study. The Journal of Comparative Neurology 290 (1):118–140CrossRefPubMed
90.
Zurück zum Zitat Yoshida M, Assimacopoulos S, Jones KR, Grove EA (2006) Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133:537–545CrossRefPubMed Yoshida M, Assimacopoulos S, Jones KR, Grove EA (2006) Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133:537–545CrossRefPubMed
91.
Zurück zum Zitat Zecevic N, Rakic P (2001) Development of layer I neurons in the primate cerebral cortex. J Neurosci 21:5607–5619PubMed Zecevic N, Rakic P (2001) Development of layer I neurons in the primate cerebral cortex. J Neurosci 21:5607–5619PubMed
92.
Zurück zum Zitat Zhao ST, Frotscher M (2010) Go or stop? Divergent roles of reelin in radial neuronal migration. Neuroscientist 16:421–434CrossRefPubMed Zhao ST, Frotscher M (2010) Go or stop? Divergent roles of reelin in radial neuronal migration. Neuroscientist 16:421–434CrossRefPubMed
93.
Zurück zum Zitat Zhao S, Chai X, Förster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117–5125CrossRefPubMed Zhao S, Chai X, Förster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117–5125CrossRefPubMed
Metadaten
Titel
Cajal-Retzius cells: organizers of cortical development
verfasst von
Werner Kilb
Michael Frotscher
Publikationsdatum
28.11.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
e-Neuroforum / Ausgabe 4/2016
Elektronische ISSN: 1868-856X
DOI
https://doi.org/10.1007/s13295-016-0031-5

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